A "more ammonium solution" to mitigate nitrogen pollution and boost crop yields
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OPINION
A “more ammonium solution” to mitigate nitrogen
OPINION
pollution and boost crop yields
G. V. Subbaraoa,1 and Timothy D. Searchingerb,1
Two of the world’s great agricultural challenges re- Because crops take up only 42 to 47% of the total ap-
quire bold new approaches and could share a solu- plied N, more than half is lost to the environment in
tion. Nitrogen (N) pollution, affecting water, air, and the some way (2, 3). Despite some recent regional improve-
climate, presents one massive challenge. Ninety percent ments in nitrogen use efficiency (NUE), global average
of increased reactive N originates as synthetic fertilizer NUE has not increased since 1980. Yet even if by 2050
applied to agricultural fields or N fixed in them (1). the world increased NUE by 50% (to ∼70%), likely 50%
We can address pollution and boost crop yields by exploiting new tools that keep a higher share of soil nitrogen as
ammonium while selecting and breeding crops to exploit an ammonium/nitrate balance. Nitrification-inhibiting traits
originally discovered in some tropical grasses can be enhanced in cereal crops too. Image credit: Flickr/CIAT.
a
Japan International Research Center for Agricultural Sciences, Ibaraki 305-8686, Japan; and bSchool of Public and International Affairs, Princeton
University, Princeton, NJ 08540
Author contributions: G.V.S. and T.D.S. shared equally in researching and writing the article; G.V.S. directed research for the additional crop testing
results described in the article.
Competing interest statement: As an active researcher on nitrification inhibition, G.V.S. could benefit from increased research funding.
Published under the PNAS license.
Any opinions, findings, conclusions, or recommendations expressed in this work are those of the authors and have not been endorsed by the
National Academy of Sciences.
1
To whom correspondence may be addressed. Email: tsearchi@princeton.edu or subbarao@jircas.affrc.go.jp.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2107576118/-/DCSupplemental.
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Published May 26, 2021.
PNAS 2021 Vol. 118 No. 22 e2107576118 https://doi.org/10.1073/pnas.2107576118 | 1 of 5increases in food production would maintain N losses to adoption rates are low and cover crops face various
the environment at roughly their present, unacceptable practical challenges (SI Appendix). To solve the N
levels (3). problem, agriculture needs additional tools to reduce
A second challenge is to increase crop yields at a this leakiness at the back end.
more rapid (linear) rate in coming decades to meet
rising food demands without clearing more forests Enter Ammonium
and releasing their carbon (3). Just as yield growth has That’s where ammonium comes in. As a cation (NH4+),
historically resulted from synergies of crop breeding ammonium adheres to most soils, particularly to clays
and management changes, future gains must rely on and SOM, and so escapes little with water. And so
doing both in even smarter ways. Large yield growth long as N remains as ammonium, it cannot generate
by adding fertilizer or doubling irrigation is no longer nitrous oxide. Benefits will occur even if nitrification is
possible or environmentally acceptable in most of the not blocked year-round. Because N2O emissions pri-
world (3–5). marily occur in the spring in many climates (SI Ap-
The scope of these challenges requires multiple pendix), even postponing nitrification for several
new approaches, and here we make the case for a weeks can reduce emissions as well as reduce fertilizer
“more ammonium solution.” With the exception of needs by reducing leaching losses. And the longer N
paddy rice, nitrate dominates the inorganic N in mod- stays in soils, particularly in the ammonium form pre-
ern agricultural soils, leading to most N pollution prob- ferred by microbes (12), the more opportunity for
lems. This solution would exploit new tools to keep a microorganisms to take it up, build soil organic car-
higher share of soil N as ammonium and select and bon, and reduce leaching (SI Appendix).
breed crops to exploit an ammonium/nitrate balance. More ammonium can also boost yields. Although
First, it’s important to ask how more ammonium too much ammonium is toxic to most crops, a fifty-year
(NH4+) and less nitrate (NO3−) would address nitrogen line of evidence has shown that a mixed share of NH4+
pollution. Although 20% of total N losses from field- and NO3− can increase cereal crop yields compared
applied N occurs through volatilization of ammonia with the near nitrate-only conditions that typically
(NH3; SI Appendix and Table 3 in 6), the great majority prevail in crop fields (13, 14). For example, in 1973,
of N losses occur after microbial reactions transform Cox and Reisenauer found that a mixture with 20%
ammonium in soils into nitrate, typically in fewer than NH4+ increased wheat growth by 54% compared with
10 days (7). As an anion, NO3− does not bind to soil all NO3− conditions (15), whereas Wang et al. in 2019
(with limited exceptions) and thus easily leaches with found >80% increases in maize growth with 25% NH4+
water into groundwater and waterways. The formation (14). As a 2002 review of ammonium toxicity wrote,
and breakdown of NO3− by bacteria and archaea also “while toxicity is observed in many species when
release nitrous oxide, a powerful greenhouse gas, as NH4+ is provided alone, . . .co-provision [with nitrate]
well as more NOx, which contributes to air pollution induces a synergistic growth response that can surpass
problems. Once N nitrifies into NO3−, unless crops or maximal growth rates on either N-source alone by as
grasses quickly take it up, it has a good chance of much as 40 to 70% in solution culture though by
polluting the environment. somewhat less in soil” (16).
Most promising strategies to reduce N pollution The precise reasons are not fully known (16, 17),
can only do so much because they focus on the “front but the benefits make sense because nitrate and
end” by reducing fertilizer application. Strategies in- ammonium each have physiological advantages and
clude educating farmers to restrict fertilizer to eco- disadvantages (13, 16–18). Plants also use mostly
nomically optimal rates, tools to help farmers apply separate systems to absorb and use nitrate and am-
most N during the growing season in amounts that monium, including different root exudates to facilitate
account for N mineralized from soils (8), and possibly root/soil interactions, different root absorption
even bacteria that help cereals fix nitrogen (9). These mechanisms, different transport pathways to leaves,
measures could increase NUE, but substantial losses and additional pathways for converting NO3− back to
will continue in part because half of global, field- NH4+ so leaves can use the N. A mix of N forms may
applied N occurs not in fertilizer but in manure, crop help plants just by allowing them to use each system.
residues, air deposition, and irrigation water (2). More In one impressive study of maize, Loussaert et al. (13)
fundamentally, applying N more carefully cannot, by found that for several weeks after silking, additional
itself, prevent N from continuing to leak at the back NO3− supply did not improve growth, but additional
end, which will continue so long as N turns into nitrate. NH4+ supply boosted maize ear growth up to 50%
Significant back-end losses will continue because (13). Saturation of the crop’s pathway to reduce NO3−
N continues to mineralize into nitrate from soil organic limited its assimilation, although the crop could still
matter (SOM) even late in growing seasons—releasing assimilate more NH4+ (13). Because rising atmo-
N absorbed into soils in previous years (SI Appendix). spheric CO2 likely inhibits plant assimilation of NO3−
Because this mineralization occurs when crops no but not NH4+, NH4+ could become even more ad-
longer take up N, it can easily turn into nitrate and vantageous in the future.
escape. In some regions most N leaching occurs in Evidence that some varieties of the same crop re-
winter when rains leach out this mineralized, inorganic spond better to ammonium than others shows genetic
N (10, 11). Cover crops provide one promising back- variation (19) and suggests that crop selection and
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end strategy for annual cropping systems, but breeding can enhance ammonium yield benefits. As
2 of 5 | PNAS Subbarao and Searchinger
https://doi.org/10.1073/pnas.2107576118 Opinion: A “more ammonium solution” to mitigate nitrogen pollution and boost
crop yieldsone illustration, we found in bench experiments that DMPP [3,4-dimethylpyrazole phosphate]) (21), and
increasing ammonium in hydroponic solution to 20 to they have severe limits: They probably do not limit
40% of total N boosted biomass production up to 60% nitrification by archaea, and effects in bacteria only
in one variety of sorghum (compared with 100% ni- inhibit the first step of conversion toward nitrate.
trate control) but caused no gains in another (SI Ap- There is no reason in principle that additional SNIs
pendix, Figs. S1 and S2). could not inhibit these other processes. Even today,
Overall, inhibiting nitrification of ammonium into one option would combine a portion of SNIs with
nitrate would not only reduce pollution but it might delayed-release compounds to extend the NI effect
also enhance yield growth in three interrelated ways: beyond a few weeks (20).
1) optimizing ammonium/nitrate ratios in soils, 2) lim- The world can also improve its use of existing SNIs.
iting N losses, and 3) supporting crop varieties bred to Varying performance reflects variability in weather but
exploit higher ammonium. probably also differences in soils, microbial commu-
nities, and crops (22). By better understanding these
New Opportunities conditions, it should be possible to improve perfor-
Agronomists have paid only modest attention to these mance by deploying SNIs for different crops and
opportunities probably because any potential to limit environmental conditions.
nitrification has appeared modest and short-lived. In BNI provides a potentially better, and lower-cost
paddy rice and some ecosystems, soil saturation alternative. As early as the 1960s, ecologists observed
causes anaerobic conditions that limit nitrification, but low nitrification rates in certain grassland and forest
most crops require aerobic conditions. Could nitrifi- ecosystems attributable to phytochemicals exuded by
cation be inhibited more and longer? In fact, many plant roots that blocked nitrification (7, 19). Yet agri-
mature ecosystems suppress nitrification and N loss to cultural breeders only began to take interest in BNI
low levels using chemicals produced by plants, soil chemicals with the discovery of low N2O emission
bacteria, and fungi (7, 19). For agriculture, the op- rates from tropical pastures of Brachiaria humidicola,
portunities include better development and use of which researchers traced to root exudation of bra-
synthetic nitrification inhibitors (SNIs) and biological chialactone (7, 19). Subsequent work by a loose net-
nitrification inhibition (BNI). work of plant researchers (SI Appendix, Table S1) has
Meta-analyses have found that existing SNIs in- been able to identify BNI traits in many staple crops
crease NUE on average by 7 to 16% and reduce N2O that include sorghum, wheat, maize, and rice (7; SI
emissions on average 35 to 40% [with larger reduc- Appendix).
tions often observed (20)]. SNIs also often lead to in- These discoveries create potential for breeding to
creases in yield by a few percent for some crops, strengthen the BNI effect and to incorporate BNI traits
enough to more than pay for their cost (20). Unfortu- into high yielding crop varieties (using classical and
nately, the effects are highly variable, which the liter- molecular breeding tools; Table 1). Wheat BNI re-
ature seems to accept as a given. search is most advanced. Without genetic engineering,
But the world does not need to settle for existing researchers have successfully transferred the chromo-
SNI formulations. Today, only three SNIs dominate some segment carrying BNI trait from a wild grass
agricultural use (nitrapyrin, DCD [dicyandiamide], and (Leymus racemosus) into cultivated wheat and are now
Table 1. BNI research status and anticipated improvements in the next 10 years
BNI Availability of Knowledge on BNI Possibility of introducing Expected level of
Crop/ characterization high-BNI chemical identity and mode BNI trait into elite crop inhibition in field (root
Pasture sp. status genetic stocks of inhibitory action cultivars (10 years from now) zone)
Brachiaria Characterized Yes Yes brachialactone, linoleic Yes 40 to 50% inhibition
sp. acid, linolenic acid -
pasture block both AMO and
grasses HAO enzymatic
pathways
Wheat Somewhat Yes No Yes 30% inhibition from first
generation BNI-
enabled wheat
cultivars
Sorghum Characterized Yes Yes sorgoleone (AMO and Yes 30% inhibition
HAO) MHPP (AMO)
Maize Work has Yes Yes (not published yet) Yes 20 to 30% inhibition
started
Rice* Somewhat Not known Yes Not known Yet to be assessed
References to "AMO" (ammonia monooxygenase) or "HAO" (hydroxylamine oxidoreductase) refer to the enzyme involved in
ntirification that is inhibited. "MHPP" refers to methyl 3 (4-hydroxyphenyl) propionate, exuded by BNI sorghum.
*Although nitrification in paddy rice fields is low, nitrification and N2O emission rates may reach extreme levels where water levels
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fluctuate (24).
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Opinion: A “more ammonium solution” to mitigate nitrogen pollution and boost crop https://doi.org/10.1073/pnas.2107576118
yieldstesting the first generation of high-yielding, BNI wheat limit their reach. BNI strength in legumes is also weak
varieties. For sorghum, research has identified the ap- or nonexistent (7); at least absent genetic engineering,
proximate chromosome region controlling sorgo- BNI is likely restricted to cereals and other grasses.
leone production, the primary BNI exudate, in efforts Potential also exists for soil nitrifying organisms to
to allow marker-assisted selection to develop high- become resistant to precise nitirification inhibiting
yielding, BNI sorghum varieties. Development of BNI proteins. But BNI has been proven persistent in nat-
agropastoral systems is in progress by exploiting the ural, tropical ecosystems (7, 19). The combination of
high BNI capacity of Brachiaria pastures in rotation multiple compounds released, plus resetting of mi-
with maize. crobial communities as a result of breaks in BNI activity
(and possibly breaks in use of BNI crops) should help
Overcoming Limitations to avoid build-up of resistance, although new breed-
BNI has potential to overcome many of the limitations ing may also become necessary.
of SNIs. Once bred into crops, farmers all over the Pursuing this solution requires policy initiatives
world can adopt them without added expense or that help overcome two challenges simultaneously—
management. And unlike SNIs (22, 23), at least some improved inhibition and crop breeding to maximize
BNI chemicals are likely effective against both nitrify- yield benefits. Scientists have little reason to pursue
ing bacteria and archaea (7, 19). either solution unless the other is also being pursued.
Although delivery of SNIs into nitrifying sites is To start, governments should fund SNI develop-
challenging, plant root systems release BNI chemicals ment, which currently has virtually no public funding.
directly into soil microsites where ammonium is most Public funding should support precommercial efforts
present and where nitrifying bacteria populate (7, 23). to develop compounds that work on both major steps
At least some plants, including sorghum, can release in the enzymatic pathways of converting ammonium
both hydrophobic BNI chemicals, which remain con- to nitrate, have multi-mode inhibition, and work on
fined to the rhizosphere, and hydrophilic BNI chem- nitrifying archaea as well as bacteria. Publicly funded
icals, which move with water flow to suppress nitrification field testing of SNIs has been more common but too
elsewhere in soils. limited to differentiate how to use them. Governments
Although SNIs can contribute to modest increases should fund large-scale, coordinated testing networks
in ammonia losses from urea unless combined with urease for different SNIs, combinations, and controlled re-
inhibitors or fertilizer is placed in a band below the surface lease formats on different crop varieties in different
soils and agroecological zones.
For BNI, the biggest need is for breeding to de-
Pursuing this solution requires policy initiatives that help velop varieties with higher BNI and that gain yield
advantages from higher ammonium. The BNI consor-
overcome two challenges simultaneously—improved
tium, founded in 2005 by Japan International Research
inhibition and crop breeding to maximize yield benefits. Center for Agricultural Sciences and three institutes of
Scientists have little reason to pursue either solution the CGIAR, has grown into a 17-institute partnership to
unless the other is also being pursued. advance BNI research (SI Appendix, Table S1). Funding
is still minimal. Private sector breeding efforts would also
be valuable for crops, such as maize, in which that sector
(20), BNI is unlikely to increase ammonia losses be- plays a prominent role.
cause they work overwhelmingly at least 10 centimeters To encourage these innovations, governments can
underground and mostly in the rhizosphere. BNI can shift farm or fertilizer subsidies to support the use of
also result from a cocktail of phytochemicals inhibiting any form of NI. Governments could legally commit
nitrifying bacteria in multiple ways (7, 19). themselves to require or subsidize BNI use up to a
Finally, the BNI effect may be able to persist in soils modest cost premium once breeds achieve a speci-
and suppress nitrification year round. For example, the fied level of effectiveness. More broadly, governments
residual BNI effect from Brachiaria pastures has sub- could vary subsidies to support any methods that reduce
N losses based on the likely level of improvement. Fer-
stantially reduced soil nitrification rates and improved
tilizer producers could also be required to sell increasing
maize grain yields for three subsequent years in a
shares of N in combination with increasingly effective
Brachiaria–maize rotation (7). Roots of other BNI crops
SNIs (20). To facilitate sales, companies would have in-
are likely to have at least some persistent effect.
centives to develop both better SNIs and more infor-
Completely stopping nitrification is neither possible
mation about how best to deploy existing SNIs.
nor beneficial for crops, but a “more ammonium so- The world will not be able to solve the nitrogen
lution” has potential to boost yields and reduce problem unless it can find ways to plug the nitrate
nitrogen pollution. leaks at the “back-end,” for which there are limited
Among challenges, the technological improve- tools. The potential emergence of BNI could repre-
ments required are by definition uncertain. Some may sent one means of doing so, while allowing crop
fear “chemical” approaches, although BNI is a natural breeding to exploit potential yield gains from a bal-
plant phenomenon, and the rhizosphere is already a ance of N forms. This combination of desirable re-
chemical battleground among plants and microbes. sults makes the case for advancing the “more
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BNI is now most effective in acidic soils, which could ammonium solution.”
4 of 5 | PNAS Subbarao and Searchinger
https://doi.org/10.1073/pnas.2107576118 Opinion: A “more ammonium solution” to mitigate nitrogen pollution and boost
crop yieldsData and Materials Availability. Further data re- provided the inspiration to develop this work. Thanks to Jacobo
garding the new wheat and sorghum experimental Arango, Michael Peters (CIAT, Colombia), Kishii Masahiro, Ivan-
Ortiz, Victor Kommerell (CIMMYT, Mexico), Santosh Deshpande,
results described in this study are available on request
and Rajeev Gupta (ICRISAT, India) for many stimulating discus-
from G.V.S. sions. This work was supported by grants to G.V.S. for BNI re-
search from MAFF (Japanese Ministry of Agriculture, Forestry,
Acknowledgments and Fisheries), JSPS (Japanese Society of Promotion of Science;
The discussions during the 3rd International BNI meeting (Octo- Grant No. 18KK0167), and WHEAT-CRP, and funding support to
ber 25–26, 2018, organized by JIRCAS at Tsukuba, Japan) T.D.S. from the Walton Family Foundation.
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